Abstract
Exposure to heavy metals can influence on metabolism, but studies have not fully evaluated young children. We investigated the association between levels of serum lead (Pb), cadmium (Cd), chromium (Cr), and arsenic (As) and risk of dyslipidemia in children. A total of 4513 children aged 6 to 9 years at 19 primary schools in Shenzhen were enrolled. Overall, 663 children with dyslipidemia were matched 1:1 with control by sex and age, and levels of serum Pb, Cd, Cr, and As were detected by inductively coupled plasma-mass spectrometry. Demographic characteristics and lifestyle were covariates in the logistic regression to determine the association of heavy metal levels with risk of dyslipidemia. Serum Pb and Cd levels were significantly higher in children with dyslipidemia than controls (133.08 vs. 84.19 μg/L; 0.45 vs. 0.29 μg/L; all P < 0.05), but this association was not found in Cr and As. We found significant upward trends for the odds ratios (ORs) of dyslipidemia associated with increasing quartiles of Pb and Cd levels (highest quartile of serum Pb OR 1.86, 95% confidence interval (CI) 1.46–2.38; Cd OR 2.51, 95% CI 1.94–3.24). Elevated serum Pb and Cd levels were associated with increased risk of dyslipidemia among children.
Similar content being viewed by others
Data availability
The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy restrictions.
References
Akhtar E, Roy AK, Haq MA, von Ehrenstein OS, Ahmed S, Vahter M, Ekstrom EC, Kippler M, Wagatsuma Y, Raqib R (2021) A longitudinal study of rural Bangladeshi children with long-term arsenic and cadmium exposures and biomarkers of cardiometabolic diseases. Environ Pollut 271:116333. https://doi.org/10.1016/j.envpol.2020.116333
Alissa EM, Ferns GA (2011) Heavy metal poisoning and cardiovascular disease. J Toxicol 2011:870125. https://doi.org/10.1155/2011/870125
Altenburger R, Backhaus T, Boedeker W, Faust M, Scholze M (2013) Simplifying complexity: mixture toxicity assessment in the last 20 years. Environ Toxicol Chem 32:1685–1687. https://doi.org/10.1002/etc.2294
Asgary S, Movahedian A, Keshvari M, Taleghani M, Sahebkar A, Sarrafzadegan N (2017) Serum levels of lead, mercury and cadmium in relation to coronary artery disease in the elderly: a cross-sectional study. Chemosphere 180:540–544. https://doi.org/10.1016/j.chemosphere.2017.03.069
Balistrieri LS, Mebane CA (2014) Predicting the toxicity of metal mixtures. Sci Total Environ 466–467:788–799. https://doi.org/10.1016/j.scitotenv.2013.07.034
Buhari O, Dayyab FM, Igbinoba O, Atanda A, Medhane F, Faillace RT (2020) The association between heavy metal and serum cholesterol levels in the US population: National Health and Nutrition Examination Survey 2009–2012. Hum Exp Toxicol 39:355–364. https://doi.org/10.1177/0960327119889654
Chai M, Li R, Ding H, Zan Q (2019) Occurrence and contamination of heavy metals in urban mangroves: a case study in Shenzhen, China. Chemosphere 219:165–173. https://doi.org/10.1016/j.chemosphere.2018.11.160
Chen Y, Qu J, Sun S, Shi Q, Feng H, Zhang Y, Cao S (2021) Health risk assessment of total exposure from cadmium in South China. Chemosphere 269:128673. https://doi.org/10.1016/j.chemosphere.2020.128673
Chowdhury R, Ramond A, O’Keeffe LM, Shahzad S, Kunutsor SK, Muka T, Gregson J, Willeit P, Warnakula S, Khan H, Chowdhury S, Gobin R, Franco OH, Di Angelantonio E (2018) Environmental toxic metal contaminants and risk of cardiovascular disease: systematic review and meta-analysis. BMJ 362:k3310. https://doi.org/10.1136/bmj.k3310
Daniels SR, Greer FR, Committee on N (2008) Lipid screening and cardiovascular health in childhood. Pediatrics 122:198–208. https://doi.org/10.1542/peds.2008-1349
Dathan-Stumpf A, Vogel M, Rieger K, Thiery J, Hiemisch A, Kiess W (2016) Serum lipid levels were related to socio-demographic characteristics in a German population-based child cohort. Acta Paediatr 105:e360–e367. https://doi.org/10.1111/apa.13438
de Burbure C, Buchet JP, Leroyer A, Nisse C, Haguenoer JM, Mutti A, Smerhovsky Z, Cikrt M, Trzcinka-Ochocka M, Razniewska G, Jakubowski M, Bernard A (2006) Renal and neurologic effects of cadmium, lead, mercury, and arsenic in children: evidence of early effects and multiple interactions at environmental exposure levels. Environ Health Perspect 114:584–590. https://doi.org/10.1289/ehp.8202
Ding W, Cheng H, Yan Y, Zhao X, Chen F, Huang G, Hou D, Mi J (2016) 10-year trends in serum lipid levels and dyslipidemia among children and adolescents from several schools in Beijing, China. J Epidemiol 26:637–645. https://doi.org/10.2188/jea.JE20140252
Fresquez MR, Pappas RS, Watson CH (2013) Establishment of toxic metal reference range in tobacco from US cigarettes. J Anal Toxicol 37:298–304. https://doi.org/10.1093/jat/bkt021
Gao Y, Li X, Dong J, Cao Y, Li T, Mielke HW (2020) Snack foods and lead ingestion risks for school aged children: a comparative evaluation of potentially toxic metals and children’s exposure response of blood lead, copper and zinc levels. Chemosphere 261:127547. https://doi.org/10.1016/j.chemosphere.2020.127547
Hamilton EM, Young SD, Bailey EH, Watts MJ (2018) Chromium speciation in foodstuffs: a review. Food Chem 250:105–112. https://doi.org/10.1016/j.foodchem.2018.01.016
He H, Pan L, Du J, Liu F, Jin Y, Ma J, Wang L, Jia P, Hu Z, Shan G (2019) Prevalence of, and biochemical and anthropometric risk factors for, dyslipidemia in children and adolescents aged 7 to 18 years in China: a cross-sectional study. Am J Hum Biol 31:e23286. https://doi.org/10.1002/ajhb.23286
Hernandez F, Bemrah N, Seby F, Noel L, Guerin T (2019) Cr(VI) and Cr(III) in milk, dairy and cereal products and dietary exposure assessment. Food Addit Contam Part B Surveill 12:209–215. https://doi.org/10.1080/19393210.2019.1598506
Holmes MV et al (2018) Lipids, lipoproteins, and metabolites and risk of myocardial infarction and stroke. J Am Coll Cardiol 71:620–632. https://doi.org/10.1016/j.jacc.2017.12.006
Ilmiawati C, Yoshida T, Itoh T, Nakagi Y, Saijo Y, Sugioka Y, Sakamoto M, Ikegami A, Ogawa M, Kayama F (2015) Biomonitoring of mercury, cadmium, and lead exposure in Japanese children: a cross-sectional study. Environ Health Prev Med 20:18–27. https://doi.org/10.1007/s12199-014-0416-4
Jadhav SH, Sarkar SN, Patil RD, Tripathi HC (2007) Effects of subchronic exposure via drinking water to a mixture of eight water-contaminating metals: a biochemical and histopathological study in male rats. Arch Environ Contam Toxicol 53:667–677. https://doi.org/10.1007/s00244-007-0031-0
Karatela S, Coomarasamy C, Paterson J, Ward NI (2019) Household smoking status and heavy metal concentrations in toenails of children. Int J Environ Res Public Health 16:3871. https://doi.org/10.3390/ijerph16203871
Kim DW, Ock J, Moon KW, Park CH (2022) Association between heavy metal exposure and dyslipidemia among Korean adults: from the Korean National Environmental Health Survey, 2015–2017. Int J Environ Res Public Health 19:3181. https://doi.org/10.3390/ijerph19063181
Lampropoulou M, Chaini M, Rigopoulos N, Evangeliou A, Papadopoulou-Legbelou K, Koutelidakis AE (2020) Association between serum lipid levels in Greek children with dyslipidemia and Mediterranean diet adherence, dietary habits, lifestyle and family socioeconomic factors. Nutrients 12:1600. https://doi.org/10.3390/nu12061600
Li T (2021) Time for a change in blood lead reference value for Chinese children. Chemosphere 267:128868. https://doi.org/10.1016/j.chemosphere.2020.128868
Li MM, Cao J, Xu J, Cai SZ, Shen XM, Yan CH (2014) The national trend of blood lead levels among Chinese children aged 0–18 years old, 1990–2012. Environ Int 71:109–117. https://doi.org/10.1016/j.envint.2014.06.005
Li Z, Xu Y, Huang Z, Wei Y, Hou J, Long T, Wang F, Cheng X, Duan Y, Chen X, Yuan H, Shen M, He M (2021) Association of multiple metals with lipid markers against different exposure profiles: a population-based cross-sectional study in China. Chemosphere 264:128505. https://doi.org/10.1016/j.chemosphere.2020.128505
Liu J, Li Y, Wang X, Gao D, Chen L, Chen M, Ma T, Ma Q, Ma Y, Zhang Y, Jiang J, Zou Z, Wang X, Dong Y, Ma J (2021) Association between fruit consumption and lipid profile among children and adolescents: a national cross-sectional study in China. Nutrients 14:63. https://doi.org/10.3390/nu14010063
Lu L, Li Y, Chen C, Zhang Y, Guo W, Zhang S, Kahe K (2022) Associations of cadmium exposure with risk of metabolic syndrome and its individual components: a meta-analysis. J Expo Sci Environ Epidemiol. https://doi.org/10.1038/s41370-022-00444-7
Mabrouk A, Bel Hadj Salah I, Chaieb W, Ben Cheikh H (2016) Protective effect of thymoquinone against lead-induced hepatic toxicity in rats. Environ Sci Pollut Res 23:12206–12215. https://doi.org/10.1007/s11356-016-6419-5
Michaud L, Sharedalal P, Seplowe M, Rosenzveig A, Frishman WH, Aronow WS (2022) Hyperlipidemia in children and adolescents. Cardiol Rev. https://doi.org/10.1097/CRD.0000000000000465
Newairy AS, Abdou HM (2009) Protective role of flax lignans against lead acetate induced oxidative damage and hyperlipidemia in rats. Food Chem Toxicol 47:813–818. https://doi.org/10.1016/j.fct.2009.01.012
Nigra AE, Ruiz-Hernandez A, Redon J, Navas-Acien A, Tellez-Plaza M (2016) Environmental metals and cardiovascular disease in adults: a systematic review beyond lead and cadmium. Curr Environ Health Rep 3:416–433. https://doi.org/10.1007/s40572-016-0117-9
Overgaard LE, Engebretsen KA, Jensen P, Johansen JD, Thyssen JP (2016) Nickel released from children’s toys is deposited on the skin. Contact Dermat 74:380–381. https://doi.org/10.1111/cod.12553
Planchart A, Green A, Hoyo C, Mattingly CJ (2018) Heavy metal exposure and metabolic syndrome: evidence from human and model system studies. Curr Environ Health Rep 5:110–124. https://doi.org/10.1007/s40572-018-0182-3
Satarug S, Garrett SH, Sens MA, Sens DA (2010) Cadmium, environmental exposure, and health outcomes. Environ Health Perspect 118:182–190. https://doi.org/10.1289/ehp.0901234
Sly PD, Flack F (2008) Susceptibility of children to environmental pollutants. Ann N Y Acad Sci 1140:163–183. https://doi.org/10.1196/annals.1454.017
Stea F, Bianchi F, Cori L, Sicari R (2014) Cardiovascular effects of arsenic: clinical and epidemiological findings. Environ Sci Pollut Res 21:244–251. https://doi.org/10.1007/s11356-013-2113-z
The Society of Pediatrics Subspecialty Group of Child Health Care, The Society of Subspecialty Group of Cardiovascular Disease, Chinese Medical Association Pediatrics, The Society of Cardiovascular Subspecialty Group of Atherosclerosis, Chinese Medical Association Disease (2009) Experts consensus for prevention and treatment of dyslipidemia in children and adolescents. Zhonghua er ke za zhi 47(6):426–428 (in Chinese)
Wang L, Martinez Steele E, Du M, Pomeranz JL, O’Connor LE, Herrick KA, Luo H, Zhang X, Mozaffarian D, Zhang FF (2021) Trends in consumption of ultraprocessed foods among US youths aged 2–19 years, 1999–2018. JAMA 326:519–530. https://doi.org/10.1001/jama.2021.10238
Wu J, Song J, Li W, Zheng M (2016a) The accumulation of heavy metals in agricultural land and the associated potential ecological risks in Shenzhen, China. Environ Sci Pollut Res 23:1428–1440. https://doi.org/10.1007/s11356-015-5303-z
Wu X, Cobbina SJ, Mao G, Xu H, Zhang Z, Yang L (2016b) A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ Sci Pollut Res 23:8244–8259. https://doi.org/10.1007/s11356-016-6333-x
Xia J, Jin C, Pan Z, Sun L, Fu Z, Jin Y (2018) Chronic exposure to low concentrations of lead induces metabolic disorder and dysbiosis of the gut microbiota in mice. Sci Total Environ 631–632:439–448. https://doi.org/10.1016/j.scitotenv.2018.03.053
Xiao L, Zhou Y, Ma J, Cao L, Wang B, Zhu C, Yang S, Li W, Zhang Z, Wang D, Guo Y, Mu G, Yuan J, Chen W (2019) The cross-sectional and longitudinal associations of chromium with dyslipidemia: a prospective cohort study of urban adults in China. Chemosphere 215:362–369. https://doi.org/10.1016/j.chemosphere.2018.10.060
Xu C, Shu Y, Fu Z, Hu Y, Mo X (2017) Associations between lead concentrations and cardiovascular risk factors in U.S. adolescents. Sci Rep 7:9121. https://doi.org/10.1038/s41598-017-09701-4
Xu H, Mao Y, Xu B, Hu Y (2021) Low-level environmental lead and cadmium exposures and dyslipidemia in adults: findings from the NHANES 2005–2016. J Trace Elem Med Biol 63:126651. https://doi.org/10.1016/j.jtemb.2020.126651
Yang D, Yang Q, Fu N, Li S, Han B, Liu Y, Tang Y, Guo X, Lv Z, Zhang Z (2021) Hexavalent chromium induced heart dysfunction via Sesn2-mediated impairment of mitochondrial function and energy supply. Chemosphere 264:128547. https://doi.org/10.1016/j.chemosphere.2020.128547
Ye Z, Chen J, Gao L, Liang Z, Li S, Li R, Jin G, Shimizu Y, Onodera SI, Saito M, Gopalakrishnan G (2020) 210Pb dating to investigate the historical variations and identification of different sources of heavy metal pollution in sediments of the Pearl River Estuary, Southern China. Mar Pollut Bull 150:110670. https://doi.org/10.1016/j.marpolbul.2019.110670
Ye L, Zhong B, Huang M, Chen W, Wang X (2021) Pollution evaluation and children’s multimedia exposure of atmospheric arsenic deposition in the Pearl River Delta, China. Sci Total Environ 787:147629. https://doi.org/10.1016/j.scitotenv.2021.147629
Yim G, Wang Y, Howe CG, Romano ME (2022) Exposure to metal mixtures in association with cardiovascular risk factors and outcomes: a scoping review. Toxics 10:116. https://doi.org/10.3390/toxics10030116
Zeng X, Xu X, Boezen HM, Huo X (2016) Children with health impairments by heavy metals in an e-waste recycling area. Chemosphere 148:408–415. https://doi.org/10.1016/j.chemosphere.2015.10.078
Zhang J, Shen H, Xu W, Xia Y, Barr DB, Mu X, Wang X, Liu L, Huang Q, Tian M (2014) Urinary metabolomics revealed arsenic internal dose-related metabolic alterations: a proof-of-concept study in a Chinese male cohort. Environ Sci Technol 48:12265–12274. https://doi.org/10.1021/es503659w
Zhang L, Shi Z, Zhang J, Jiang Z, Wang F, Huang X (2015) Spatial and seasonal characteristics of dissolved heavy metals in the east and west Guangdong coastal waters, South China. Mar Pollut Bull 95:419–426. https://doi.org/10.1016/j.marpolbul.2015.03.035
Zhao M, Yin G, Xu J, Ge X, Li A, Mei Y, Wu J, Liu X, Wei L, Xu Q (2023) Independent, combine and interactive effects of heavy metal exposure on dyslipidemia biomarkers: a cross-sectional study in northeastern China. Ecotoxicol Environ Saf 250:114494. https://doi.org/10.1016/j.ecoenv.2022.114494
Zhu X, Fan Y, Sheng J, Gu L, Tao Q, Huang R, Liu K, Yang L, Chen G, Cao H, Li K, Tao F, Wang S (2021) Association between blood heavy metal concentrations and dyslipidemia in the elderly. Biol Trace Elem Res 199:1280–1290. https://doi.org/10.1007/s12011-020-02270-0
Acknowledgements
The authors gratefully acknowledge all the doctors and nurses in the Department of Laboratory Medicine, Baoan Central Hospital, Shenzhen. The authors also thank all the school doctors and teachers in Baoan District who participated in the survey.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. The experiments were conceived and designed by Qingying Zhang. Material preparation was performed by Yingbin You. Data collection and analysis were performed by Shufan Li, Ruiguo Liu, Yueyang Wu, Rimei Liang, Zhijiang Zhou, and Jiaqi Chen. Methodology guidance was provided by Pi Guo. The first draft of the manuscript was written by Shufan Li, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
The study was approved by the Ethics Committee of Baoan Central Hospital of Shenzhen (protocol code IRB-PJ-2018–002) and was performed according to the Declaration of Helsinki. Participation was voluntary, and written informed consent was obtained from all parents of the participants before enrolment.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, S., Liu, R., Wu, Y. et al. Elevated serum lead and cadmium levels associated with increased risk of dyslipidemia in children aged 6 to 9 years in Shenzhen, China. Environ Sci Pollut Res 30, 70558–70568 (2023). https://doi.org/10.1007/s11356-023-27335-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-27335-0